Skeletal progenitor/stem cells (SSCs) play a critical role in postnatal bone growth and maintenance. Telomerase (Tert) activity prevents cellular senescence and is required for maintenance of stem cells in self‐renewing tissues. Here we investigated the role of mTert‐expressing cells in postnatal mouse long bone and found that mTert expression is enriched at the time of adolescent bone growth. mTert‐GFP+ cells were identified in regions known to house SSCs, including the metaphyseal stroma, growth plate, and the bone marrow. We also show that mTert‐expressing cells are a distinct SSC population with enriched colony‐forming capacity and contribute to multiple mesenchymal lineages, in vitro. In contrast, in vivo lineage‐tracing studies identified mTert+ cells as osteochondral progenitors and contribute to the bone‐forming cell pool during endochondral bone growth with a subset persisting into adulthood. Taken together, our results show that mTert expression is temporally regulated and marks SSCs during a discrete phase of transitional growth between rapid bone growth and maintenance.